Aquaculture changes the profile of antibiotic resistance and mobile genetic element associated genes in Baltic Sea sediments

FEMS Microbiology Ecology

Volumn 92, Issue 4, 2016, Pages

  Muziasari, Windi I ^a   Pärnänen, Katariina ^a   Johnson, Timothy A ^b,c,d   Lyra, Christina ^a   Karkman, Antti ^a   Stedtfeld, Robert D ^c   Tamminen, Manu ^e,f   Tiedje, James M ^c   Virta, Marko ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

^b MCMASTER UNIVERSITY   (Canada)

^c Michigan State University   (United States)

^d NATIONAL ANIMAL DISEASE CENTER   (United States)

^e ETH ZURICH   (Switzerland)

^f SWISS FEDERAL INSTITUTE OF AQUATIC SCIENCE AND TECHNOLOGY   (Switzerland)

Author keywords

Baltic Sea; environmental resistome; fish farms; mobile genetic elements; qPCR array; transposons

Indexed keywords

AMINOGLYCOSIDE; ANTIINFECTIVE AGENT; BETA LACTAM; RNA 16S;

ANIMAL; ANTIBIOTIC RESISTANCE; AQUACULTURE; BACTERIAL GENE; BACTERIUM; DRUG EFFECTS; FINLAND; FISHERY; GENETICS; INTEGRON; INTERSPERSED REPEAT; MICROBIAL SENSITIVITY TEST; MICROBIOLOGY; POLYMERASE CHAIN REACTION; PROCEDURES; SEA; SEDIMENT;

AMINOGLYCOSIDES; ANIMALS; ANTI-BACTERIAL AGENTS; AQUACULTURE; BACTERIA; BETA-LACTAM RESISTANCE; BETA-LACTAMS; DRUG RESISTANCE, BACTERIAL; FINLAND; FISHERIES; GENES, BACTERIAL; GEOLOGIC SEDIMENTS; INTEGRONS; INTERSPERSED REPETITIVE SEQUENCES; MICROBIAL SENSITIVITY TESTS; OCEANS AND SEAS; POLYMERASE CHAIN REACTION; RNA, RIBOSOMAL, 16S;

EID: 85015992441     PISSN: 01686496     EISSN: 15746941     Source Type: Journal    
DOI: 10.1093/femsec/fiw052     Document Type: Article

References (38)

1. Amann RI, Ludwig W, Schleifer KH. Phylogenetics identification and in-situ detection of individual microbial cells without cultivation. Microbiol Rev 1995;59:143–69.
2. Andersson DI, Hughes D. Microbiological effects of sublethal levels of antibiotics. Nat Rev Microbiol 2014;12:465–78.
3. Bhullar K, Waglechner N, Pawlowski A et al. Antibiotic resistance is prevalent in an isolated cave microbiome. PLoS ONE 2012;7:e34953.
4. Buschmann AH, Tomova A, López A et al. Salmon aquaculture and antimicrobial resistance in the marine environment. PLoS ONE 2012;7:1–11.
5. Cabello FC, Godfrey HP, Tomova A et al. Antimicrobial use in aquaculture re-examined: its relevance to antimicrobial resistance and to animal and human health. Environ Microbiol 2013;15:1917–42.
6. Chelossi E, Vezzulli L, Milano A et al. Antibiotic resistance of benthic bacteria in fish-farm and control sediments of the Western Mediterranean. Aquacult 2003;219:83–97.
7. Chen B, Yang Y, Liang X et al. Metagenomic Profiles of Antibiotic Resistance Genes (ARGs) between Human Impacted Estuary and Deep Ocean Sediments. Environ Sci Technol 2013;47:12753–60.
8. Food and Agriculture Organization (FAO). Responsible Use of Antibiotics in Aquaculture. 2006, http://www.fao.org/3/a-a0282e.pdf (10 March 2016, date last accessed).
9. Food and Agriculture Organization (FAO). Cage Aquaculture—Regional Reviews and Global Overview. 2007, ftp://ftp.fao.org/docrep/fao/010/a1290e/a1290e02.pdf (10 March 2016, date last accessed).
10. Gao P, Mao D, Luo Y et al. Occurrence of sulfonamide and tetracycline-resistant bacteria and resistance genes in aquaculture environment. Water Res 2012;46:2355–64.
11. Gaze WH, Zhang L, Abdouslam NA et al. Impacts of anthropogenic activity on the ecology of class 1 integrons and integron-associated genes in the environment. ISME J 2011;5:1253–61.
12. Giraud E, Douet DG, Le Bris H et al. Survey of antibiotic resistance in an integrated marine aquaculture system under oxolinic acid treatment. FEMS Microbiol Ecol 2006;55:439–48.
13. Groh JL, Luo Q, Ballard JD et al. Genes that enhance the ecological fitness of Shewanella oneidensis MR-1 in sediments reveal the value of antibiotic resistance. Appl Environ Microb 2007;73:492–8.
14. Gullberg E, Cao S, Berg OG et al. Selection of resistant bacteria at very low antibiotic concentrations. PLoS Pathog 2011;7:1–9.
15. Heuer OE, Kruse H, Grave K et al. Human health consequences of use of antimicrobial agents in aquaculture. Clin Infect Dis 2009;49:1248–53.
16. Knapp C, Engemann C, Hanson ML et al. Indirect evidence of transposon-mediated selection of antibiotic resistance genes in aquatic systems at low-level oxytetracycline exposures. Environ Sci Technol 2008;42:5348–53.
17. Liebert CA, Hall RM, Summers AO. Transposon Tn21, flagship of the floating genome. Microbiol Mol Biol R 1999; 63:507–22.
18. Looft T, Johnson TA, Allen HK et al. In-feed antibiotic effects on the swine intestinal microbiome. P Natl Acad Sci 2012;109:1691–6.
19. Martinez JL, Coque TM, Baquero F. What is a resistance gene? Ranking risk in resistomes. Nat Rev Microbiol Advance online publication. Nat Rev Microbiol 2015;13:116–23.
20. Martinez JL, Fajardo A, Garmendia L et al. A global view of antibiotic resistance. FEMS Microbiol Rev 2009;33:44–65.
21. Mente E, Pierce GJ, Santos MB et al. Effect of feed and feeding in the culture of salmonids on the marine aquatic environment: a synthesis for European aquaculture. Aquacult Int 2006;14:499–522.
22. Muziasari WI, Managaki S, Pärnänen K et al. Sulfonamide and trimethoprim resistance genes persist in sediments at Baltic Sea aquaculture farms but are not detected in the surrounding environment. PLoS ONE 2014;9:e92702.
23. Oksanen J, Blanchet FG, Kindt R et al. Vegan: Community Ecology Package. R package version 2.2-0. 2014, http://CRAN.Rproject.org/package=vegan (10 March 2016, date last accessed).
24. Partridge SR, Tsafnat G, Coiera E et al. Gene cassettes and cassette arrays in mobile resistance integrons. FEMS Microbiol Rev 2009;33:757–84.
25. Pitkanen LK, Tamminen M, Hynninen A et al. Fish farming affects the abundance and diversity of the mercury resistance gene merA in marine sediments. Microbes Environ 2011;26: 205–11.
26. Roe MT, Veda E, Pillai SD. Antimicrobial resistance markers of class 1 and class 2 integron-bearing Escherichia coli from irrigation water and sediments. Emerg Infect Dis 2003;9:822–6.
27. Sapkota A, Sapkota AR, Kucharski M et al. Aquaculture practices and potential human health risks: current knowledge and future priorities. Environ Int 2008;34:1215–26.
28. Schmittgen TD, Livak JK. Analyzing real-time PCR data by the comparative Ct method. Nat Protoc 2008;3:1101–8.
29. Segawa T, Takeuchi N, Rivera A et al. Distribution of antibiotic resistance genes in glacier environments. Environ Microbiol Rep 2013;5:127–34.
30. Sorum H. Mobile drug resistance genes among fish bacteria. Acta Path Micro Im 1998;106:74–6.
31. Sundin GW. Distinct recent lineages of the strA-strB streptomycin-resistance genes in clinical and environmental bacteria. Curr Microbiol 2002;45:63–9.
32. Sundin GW, Bender CL. Dissemination of the strA-strB streptomycin-resistance genes among commensal and pathogenic bacteria from humans, animals, and plants. Mol Ecol 1996;5:133–43.
33. Tamminen M, Karkman A, Corander J et al. Differences in bacterial community composition in Baltic Sea sediment in response to fish farming. Aquacult 2011a;313:15–23.
34. Tamminen M, Karkman A, Lõhmus A et al. Tetracycline resistance genes persist at aquaculture farms in the absence of selection pressure. Environ Sci Technol 2011b;45: 386–91.
35. Wang FH, Qiao M, Su JQ et al. High throughput profiling of antibiotic resistance genes in urban park soils with reclaimed water irrigation. Environ Sci Technol 2014;48:9079–85.
36. Xiong W, Sun Y, Zhang T et al. Antibiotics, antibiotics resistance genes, and bacterial community composition in fresh water aquaculture environment in China. Microb Ecol 2015;70: 425–32.
37. Yang J, Wang C, Shu C et al. Marine sediment bacteria harbor antibiotic resistance genes highly similar to those found in human pathogens. Microb Ecol 2013;65:975–81.
38. Zhu YG, Johnson TA, Su JQ et al. Diverse and abundant antibiotic resistance genes in Chinese swine farms. P Natl Acad Sci 2013;110:3435–40.